Research

Most of my research reflects my fascination with variation in species interactions. As biologists attempt to quantify and predict the ecological and evolutionary consequences of species interactions, they often have to cope with high levels of variation. My work on variation in interaction strength seeks to accurately predict the results of interactions among arthropods in highly connected food webs. This work addresses fundamental questions in community ecology (the relationship between biodiversity and interaction strength, the relative strength of positive species interactions, etc.) while also providing the means to predict the outcome of complex interactions in managed systems. My work on the evolutionary ecology of plant-insect interactions is focused on the effect of genetic variation on these interactions. My collaborators and I have found that changes in the level of genetic variation within plant populations can alter interactions between plants and their enemies. This work is highly relevant to the conservation of rare plants and to understanding the evolution of plant mating systems.

Research To Date

Effects of Complex Trophic Interactions on Community Structure and Plant Fitness
For the past several years, my students, research assistants, and I have used the red imported fire ant, Solenopsis invicta, as a model system for studying complex trophic interactions. Although notoriously abundant and widespread in the southeastern U.S., surprisingly few studies have documented their effects on other arthropods and plants. My graduate students Chad Harvey, Ian Kaplan, John Styrsky, Laura Cooper and I have taken a comparative approach to this study by evaluating the effects of fire ants in four agricultural crops. We found that red imported fire ants are major predators of both predaceous arthropods and herbivorous insects, but that the effects of fire ants vary widely within and among different crops. In cotton, for example, fire ants often dramatically suppress the densities of other arthropods, but do not in soybean, even though fire ants are more abundant in soybean fields than in cotton fields. Our most recent work suggests that a facultative mutualism between fire ants and honeydew-producing aphids explains much of the variation in the effects of fire ants. In the absence of aphids, fire ants have relatively weak effects on other arthropods. In the presence of aphids, however, fire ants are extremely aggressive and fire ant predation of both predaceous and herbivorous arthropods significantly increases. Hosting this mutualism may be beneficial for many plant species because aphids cause relatively little damage to most plants, but the caterpillars and true bugs that are affected by the mutualism routinely reduce plant fitness. Our results suggest that a positive species interaction, in this case a facultative mutualism, may explain much of the variation in a food web that contains dozens of interacting species. We are beginning to extend our study to the landscape level by investigating how fire ant – aphid mutualisms affect the movement of aphid-vectored plant viruses.

Effects of Inbreeding (Self-Pollination) in Plants on Plant-Natural Enemy Interactions
This is a collaborative project with Dr. David Carr of the University of Virginia to study the effects of inbreeding on plant-natural enemy interactions. By reducing heterozygosity within individuals, inbreeding alters the distribution of genetic variation, increases the expression of recessive alleles, and reduces the contribution of overdominance. Our collaboration started by examining the effect of self- and cross-pollination in the yellow monkeyflower, Mimulus guttatus (Scrophulariaceae), on tolerance to and host plant quality for a xylem-feeding spittlebug. We found that inbreeding exacerbated the detrimental effects of spittlebugs and altered host plant quality for spittlebugs. My graduate student Joel Tindle is quantifying changes in plant defensive traits associated with inbreeding. Joel’s work suggests that inbred monkeyflowers increase their investment in trichomes to counter their reduced tolerance of herbivory. My former graduate student Helen Hull-Sanders asked similar questions using the entire-leaf morning glory, Ipomoea hederacea, and a suite of herbivores that feed on this plant. Helen found that inbreeding in entire-leaf morning glories altered interactions with insect herbivores, but that the effects of inbreeding on resistance and tolerance varied with the feeding habit (leaf chewer versus phloem feeder) of the herbivore. Furthermore, Helen found that plant defense theory could accurately predict variation in the effects of inbreeding on morning glory-herbivore interactions. We have also investigated the effects of inbreeding on plant defense against pathogens in M. guttatus. In a collaborative study with Dr. John Murphy, a plant virologist at Auburn University, we found that inbred plants infected with Cucumber mosaic virus (CMV) had proportionally greater fitness loss than infected outbred plants. Taken together, the results of our work suggest that inbreeding by plants can have important effects on the dynamics of plant-natural enemy interactions and that the magnitude and direction of these effects may be predictable.

Evolution of Omnivory in Heteropteran Insects
Omnivory is a widespread feeding habit in animals and studies of the ecological consequences of omnivory are proliferating (e.g., a recent Special Feature in Ecology highlighted work in this area). Few studies, however, have investigated the evolutionary origin of omnivory, the selective forces that promote or constrain omnivory, and the morphological, physiological, and behavioral hurdles that animals must overcome to become omnivores. My collaborators and I focused on the terrestrial lineages of the insect order Heteroptera and used life history data and recent phylogenies to test two hypotheses concerning the evolutionary origin of feeding on both plants and prey. We found strong evidence that insects that feed on nitrogen-rich plant parts (seed and pollen) and insects that have broad host ranges (polyphagous) are much more likely to evolve the ability to feed on mixed diets of plant and prey. We hope this study stimulates further development of ideas concerning the evolutionary origin of this important feeding habit.

Host-Race Formation in a Stem- and Gall-Boring BeetleDr. Warren Abrahamson and I studied a host shift and potential host-race formation by a tumbling flower beetle associated with two species of goldenrod in the eastern United States. Mordellistena convicta (Coleoptera: Mordellidae) is a facultative predator found in the galls induced by the tephritid fly, Eurosta solidaginis, on two species of goldenrod. We found that M. convicta may have recently undergone a host shift and subsequent host-race formation as a result of a previous shift by Eurosta. Our work suggests that some specialized natural enemies may differentiate in parallel with their herbivorous prey during host shifts.

Ecological Consequences of Omnivory
My dissertation research focused on the ecological consequences of feeding at multiple trophic levels. I quantified the effect of omnivory on the abundance and distribution of an omnivorous insect and two of its prey species. I found that omnivory by big-eyed bugs, Geocoris punctipes, intensified the interaction between big-eyed bugs and prey (aphids and moth eggs). The impact of big-eyed bugs on prey, however, was mediated by host plant quality.

Future Research Programs

Community and Landscape Level Consequences of Complex Trophic Interactions I plan to continue studying species interactions in arthropod food webs. The long-term goal of this research is to find key interactions that explain a disproportionately large amount of variation in the abundance and distribution of species. This type of work is important if we are to accurately predict the outcome of species interactions in diverse and highly connected communities. In the near future I plan on experimentally addressing questions such as what are the effects of biodiversity on the number and strength of species interactions and what are the effects of ant – aphid mutualisms on the spread of aphid-vectored viruses. Our hypothesis is that aphid ‘tending’ by fire ants leads to larger aphid populations that are more likely to disperse and spread plant viruses. As this project develops I hope to tackle fundamental issues in community ecology as well as ask novel questions about species interactions.

Effects of Herbivory on the Evolution of Plant Mating Systems This project will continue my collaboration with Dr. David Carr. We will focus our future work on the effects of herbivory on the evolution and maintenance of mixed mating systems in plants. Evolutionary ecologists have been interested in the evolution of cross-pollination and the maintenance of mixed mating systems (plant species where some individuals outcross and some self) since at least the 1850’s. Selfing has two benefits that should result in strong selection for self-pollination in natural plant populations. First, selfing provides reproductive assurance for plants when pollinators or mates are rare. Second, plants that self and outcross have a 50% gene transmission advantage over plants that strictly cross-pollinate. These advantages suggest that selfing should be widespread in higher plants. Cross-pollination, however, is the predominant mating system in higher plants. It is believed that the primary cost of self-fertilization, the reduced fitness of inbred progeny relative to outbred progeny (inbreeding depression), is the major impediment to the evolution of selfing in plants. When inbreeding depression is greater than the fitness advantages of selfing, there should be selection for cross-pollination. Our previous work demonstrated that insect herbivory, an important ecological interaction for almost all plant species, can increase or decrease inbreeding depression. This suggests that insect herbivory could play a strong role in the evolutionary dynamics of plant mating systems. We are beginning to develop and test a quantitative model that incorporates the effects of herbivory on inbreeding depression to predict the evolutionary dynamics of mating systems.

The Evolution of Omnivory
I hope to build on my previous work in this area in collaboration with an insect systematist. I have identified several Heteropteran groups where omnivory has evolved within ancestrally herbivorous lineages and other groups where omnivory has evolved within ancestrally predaceous lineages. I would like to use these ‘transitional’ groups to test several ideas about the evolution of omnivory and the evolutionary and ecological consequences of omnivory.

The Interactive Effects of Herbivores and Plant Pathogens
Plants are often simultaneously attacked by insect herbivores and plant pathogens and recent studies suggest that these two types of natural enemies can have interactive effects on plant fitness. My collaborators and I recently investigated the interactive effects of spittlebugs and a plant virus (CMV) on the fitness of M. guttatus plants. We found strong evidence that spittlebugs and CMV interacted to affect plant fitness and that genetic variation underlies the degree and direction of this interaction. This suggests that selection can act on the interaction between the two enemies and that strong selection imposed by one will alter the response of M. guttatus populations to the second. I would like to expand this work in the future and quantify some of the mechanisms underlying the interactive effect of spittlebugs and CMV and study the evolutionary dynamics associated with selection imposed by these two types of natural enemies.

Extending the Elemental Defense Hypothesis
Plants growing under natural conditions often vary greatly in their tissue metal concentrations. Plant species that live on mineralized or ultramafic (high metal) soils, for example, often accumulate or even hyperaccumulate these metals into their tissue. It has been proposed that high concentrations of metals may act as an ‘elemental defense’ that protects plants from herbivores. Dr. Robert Boyd of Auburn University has been a pioneer in the development and initial testing of this idea. For example, work in the Boyd lab has shown that hyperaccumulated levels of Ni (>1,000 mg/g of plant tissue) can protect Ni hyperaccumulating plants such as Streptanthus polygaloides from a wide variety of herbivorous arthropods. I have recently collaborated with Dr. Boyd’s group to test the idea that elevated metal concentrations far lower than those found in hyperaccumulating plants can provide defense against insect herbivores. It was originally thought, however, that ‘elemental defense’ may only be important in the 500 or so plant species that hyperaccumulate metals. Our results using caterpillars fed artificial diet amended with various metals strongly support this hypothesis and that metal concentrations as low as 20 (mg/g of plant tissue) may provide protection against herbivores. This study suggests that ‘elemental defense’ may be far more widespread in plants than previously thought because thousands of plant species have moderately elevated metal concentrations. I hope to test this hypothesis in the greenhouse and in the field using several species of native plants that live on mineralized soils and are believed to have elevated levels of metals.

The Role of Phenotypic Plasticity in Averting ‘Evolutionary Dead Ends’
Most species of Mimulus live in ephemerally wet habitats where soil moisture, herbivory, light, and other environmental factors fluctuate dramatically in space and time. Variation in these traits strongly affects the fitness of Mimulus plants and out-crossing species of Mimulus have high levels of genetic variation associated with the response to these variables. Several species of Mimulus that live in these habitats, however, only self pollinate (e.g., M. micranthus). Populations of these plants typically have relatively low genetic diversity and low potential to respond to selection. Populations of these plants, however, appear to be as persistent as populations of out-crossing Mimulus taxa. How can populations of these strictly selfing plants persist in such highly variable environments? An intriguing possibility is that strictly selfing Mimulus species have evolved unusually high levels of phenotypic plasticity. I hope to test this hypothesis in the future by measuring the response of out-crossing and strictly selfing Mimulus taxa to varying regimes of soil moisture and herbivory. Mimulus is an excellent group for this study because this genus contains multiple species that out-cross and multiple species that only self-pollinate.